Distinct mechanisms underlie oral vs aboral regeneration in the cnidarian Hydractinia echinata

Abstract

Cnidarians possess remarkable powers of regeneration, but the cellular and molecular mechanisms underlying this capability are unclear. Studying the hydrozoan Hydractinia echinata we show that a burst of stem cell proliferation occurs following decapitation, forming a blastema at the oral pole within 24 hr. This process is necessary for head regeneration. Knocking down Piwi1, Vasa, Pl10 or Ncol1 expressed by blastema cells inhibited regeneration but not blastema formation. EdU pulse-chase experiments and in vivo tracking of individual transgenic Piwi1 ⁺ stem cells showed that the cellular source for blastema formation is migration of stem cells from a remote area. Surprisingly, no blastema developed at the aboral pole after stolon removal. Instead, polyps transformed into stolons and then budded polyps. Hence, distinct mechanisms act to regenerate different body parts in Hydractinia. This model, where stem cell behavior can be monitored in vivo at single cell resolution, offers new insights for regenerative biology.

DOI: http://dx.doi.org/10.7554/eLife.05506.001

eLife digest

Although all animals are capable of regenerating damaged tissue to some extent, a few—including jellyfish, coral, and their relatives—are able to regenerate entire lost body parts. Closely related species may have very different regeneration capabilities. This has led some researchers to propose that higher animals, such as mammals, still possess the ancient genes that allow entire body parts to regenerate, but that somehow the genes have been disabled during their evolution. Studying animals that can regenerate large parts of their bodies may therefore help scientists understand what prevents others, including humans, from doing so.

An animal that is particularly useful for studies into regeneration is called Hydractinia echinata. These tiny marine animals make their homes on the shells of hermit crabs. They are small, transparent and stay fixed to one spot, making it easy for scientists to grow them in the laboratory and closely observe what is going on when they regenerate.

Bradshaw et al. genetically engineered Hydractinia individuals to produce a fluorescent protein in their stem cells; these cells have the ability to become one of several kinds of mature cell, and often help to repair and grow tissues. This allowed the stem cells to be tracked using a microscope.

When the head of Hydractinia was cut off, stem cells in the animals' mid body section migrated to the end where the head used to be and multiplied. These stem cells then created a bud (known as a blastema) that developed into a new, fully functional head within two days, allowing the animals to capture prey. Reducing the activity of certain stem cell genes prevented the new head from growing, but the bud still formed.

Next, Bradshaw et al. removed a structure from the opposite end of the animal, called the stolon, which normally helps Hydractinia attach to hermit crabs shells. Stolons regenerated in a completely different way to heads. No bud formed. Instead, the remainder of the animal's body, which included the head and the body column, gradually transformed into a stolon rather than regenerating this structure, and only then grew a new body column and head. Therefore, different tissues in the same animal can regenerate in different ways. Understanding the ‘tricks’ used by animals like Hydractinia to regenerate may help translate these abilities to regenerative medicine.

DOI: http://dx.doi.org/10.7554/eLife.05506.002